Genetic variation in the cellular response of Daphnia magna (Crustacea: Cladocera) to its bacterial parasite

Abstract

Linking measures of immune function with infection, and ultimately, host and parasite fitness is a major goal in the field of ecological immunology. In this study, we tested for the presence and timing of a cellular immune response in the crustacean Daphnia magna following exposure to its sterilizing endoparasite Pasteuria ramosa. We found that D. magna possesses two cell types circulating in the haemolymph: a spherical one, which we call a granulocyte and an irregular-shaped amoeboid cell first described by Metchnikoff over 125 years ago. Daphnia magna mounts a strong cellular response (of the amoeboid cells) just a few hours after parasite exposure. We further tested for, and found, considerable genetic variation for the magnitude of this cellular response. These data fostered a heuristic model of resistance in this naturally coevolving host-parasite interaction. Specifically, the strongest cellular responses were found in the most susceptible hosts, indicating resistance is not always borne from a response that destroys invading parasites, but rather stems from mechanisms that prevent their initial entry. Thus, D. magna may have a two-stage defence--a genetically determined barrier to parasite establishment and a cellular response once establishment has begun.

Figure 1.

Differential interference contrast image of an amoeboid haemocyte from D. magna. Scale bar, 5 µm.

Figure 2.

Haemocyte counts per host in P. ramosa-exposed and control D. magna (filled and open symbols, respectively; n = 6 and each replicate consists of five Daphnia). Error bars are 1 s.e.m. See table 1 for statistical details.

Figure 3.

Fold induction of haemocyte numbers in P. ramosa-exposed D. magna (n = 6, each replicate consists of five Daphnia), relative to unexposed D. magna (n = 6, each replicate consists of five Daphnia). The bold line at y = 1 shows the uninduced (basal) level. The inset shows the proportion of individuals that became infected in P. ramosa-exposed treatments in each genotype (n = 12, each replicate consists of an individual Daphnia). Asterisks indicate if haemocyte numbers rose significantly (after sequential Bonferroni adjustment) above basal levels: ** p < 0.01, *** p < 0.001.